Jawbone microenvironment promotes periodontium regeneration by regulating the function of periodontal ligament stem cells
Identifieur interne : 000840 ( Pmc/Curation ); précédent : 000839; suivant : 000841Jawbone microenvironment promotes periodontium regeneration by regulating the function of periodontal ligament stem cells
Auteurs : Bin Zhu [République populaire de Chine] ; Wenjia Liu [République populaire de Chine] ; Yihan Liu [République populaire de Chine] ; Xicong Zhao [République populaire de Chine] ; Hao Zhang [République populaire de Chine] ; Zhuojing Luo [République populaire de Chine] ; Yan Jin [République populaire de Chine]Source :
- Scientific Reports [ 2045-2322 ] ; 2017.
Abstract
During tooth development, the jawbone interacts with dental germ and provides the development microenvironment. Jawbone-derived mesenchymal stem cells (JBMSCs) maintain this microenvironment for root and periodontium development. However, the effect of the jawbone microenvironment on periodontium tissue regeneration is largely elusive. Our previous study showed that cell aggregates (CAs) of bone marrow mesenchymal stem cells promoted periodontium regeneration on the treated dentin scaffold. Here, we found that JBMSCs enhanced not only the osteogenic differentiation of periodontal ligament stem cells (PDLSCs) but also their adhesion to titanium (Ti) material surface. Importantly, the compound CAs of PDLSCs and JBMSCs regenerated periodontal ligament-like fibers and mineralized matrix on the Ti scaffold surface, both in nude mice ectopic and minipig orthotopic transplantations. Our data revealed that an effective regenerative microenvironment, reconstructed by JBMSCs, promoted periodontium regeneration by regulating PDLSCs function on the Ti material.
Url:
DOI: 10.1038/srep40088
PubMed: 28053317
PubMed Central: 5215380
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Fourth Military Medical University</institution>, Xi’an, Shaanxi,<country>People’s Republic of China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="a4"><institution>Department of Stomatology</institution>, PLA 301th Hospital, Beijing,<country>People’s Republic of China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Zhao, Xicong" sort="Zhao, Xicong" uniqKey="Zhao X" first="Xicong" last="Zhao">Xicong Zhao</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>State Key Laboratory of Military Stomatology, Centre for Tissue Engineering, School of Stomatology, Fourth Military Medical University</institution>, Xi’an, Shaanxi,<country>People’s Republic of China</country></nlm:aff><country 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Republic of China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Jin, Yan" sort="Jin, Yan" uniqKey="Jin Y" first="Yan" last="Jin">Yan Jin</name><affiliation wicri:level="1"><nlm:aff id="a1"><institution>State Key Laboratory of Military Stomatology, Centre for Tissue Engineering, School of Stomatology, Fourth Military Medical University</institution>, Xi’an, Shaanxi,<country>People’s Republic of China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Scientific Reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>During tooth development, the jawbone interacts with dental germ and provides the development microenvironment. Jawbone-derived mesenchymal stem cells (JBMSCs) maintain this microenvironment for root and periodontium development. However, the effect of the jawbone microenvironment on periodontium tissue regeneration is largely elusive. Our previous study showed that cell aggregates (CAs) of bone marrow mesenchymal stem cells promoted periodontium regeneration on the treated dentin scaffold. Here, we found that JBMSCs enhanced not only the osteogenic differentiation of periodontal ligament stem cells (PDLSCs) but also their adhesion to titanium (Ti) material surface. Importantly, the compound CAs of PDLSCs and JBMSCs regenerated periodontal ligament-like fibers and mineralized matrix on the Ti scaffold surface, both in nude mice ectopic and minipig orthotopic transplantations. Our data revealed that an effective regenerative microenvironment, reconstructed by JBMSCs, promoted periodontium regeneration by regulating PDLSCs function on the Ti material.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Slavkin, H C" uniqKey="Slavkin H">H. C. Slavkin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Luan, X" uniqKey="Luan X">X. Luan</name></author><author><name sortKey="Ito, Y" uniqKey="Ito Y">Y. Ito</name></author><author><name sortKey="Diekwisch, T G" uniqKey="Diekwisch T">T. G. Diekwisch</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Thesleff, I" uniqKey="Thesleff I">I. Thesleff</name></author><author><name sortKey="Vaahtokari, A" uniqKey="Vaahtokari A">A. Vaahtokari</name></author><author><name sortKey="Kettunen, P" uniqKey="Kettunen P">P. Kettunen</name></author><author><name sortKey="Aberg, T" uniqKey="Aberg T">T. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Sci Rep</journal-id><journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id><journal-title-group><journal-title>Scientific Reports</journal-title></journal-title-group><issn pub-type="epub">2045-2322</issn><publisher><publisher-name>Nature Publishing Group</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28053317</article-id><article-id pub-id-type="pmc">5215380</article-id><article-id pub-id-type="pii">srep40088</article-id><article-id pub-id-type="doi">10.1038/srep40088</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Jawbone microenvironment promotes periodontium regeneration by regulating the function of periodontal ligament stem cells</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Zhu</surname><given-names>Bin</given-names></name><xref ref-type="aff" rid="a1">1</xref><xref ref-type="aff" rid="a2">2</xref><xref ref-type="aff" rid="a3">3</xref><xref ref-type="author-notes" rid="n1">*</xref></contrib><contrib contrib-type="author"><name><surname>Liu</surname><given-names>Wenjia</given-names></name><xref ref-type="aff" rid="a1">1</xref><xref ref-type="author-notes" rid="n1">*</xref></contrib><contrib contrib-type="author"><name><surname>Liu</surname><given-names>Yihan</given-names></name><xref ref-type="aff" rid="a1">1</xref><xref ref-type="aff" rid="a4">4</xref><xref ref-type="author-notes" rid="n1">*</xref></contrib><contrib contrib-type="author"><name><surname>Zhao</surname><given-names>Xicong</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Zhang</surname><given-names>Hao</given-names></name><xref ref-type="aff" rid="a1">1</xref></contrib><contrib contrib-type="author"><name><surname>Luo</surname><given-names>Zhuojing</given-names></name><xref ref-type="corresp" rid="c1">a</xref><xref ref-type="aff" rid="a2">2</xref></contrib><contrib contrib-type="author"><name><surname>Jin</surname><given-names>Yan</given-names></name><xref ref-type="corresp" rid="c2">b</xref><xref ref-type="aff" rid="a1">1</xref></contrib><aff id="a1"><label>1</label><institution>State Key Laboratory of Military Stomatology, Centre for Tissue Engineering, School of Stomatology, Fourth Military Medical University</institution>, Xi’an, Shaanxi,<country>People’s Republic of China</country></aff><aff id="a2"><label>2</label><institution>Department of Orthopedics Surgery, Xijing Hospital, Fourth Military Medical University</institution>, Xi’an, Shaanxi,<country>People’s Republic of China</country></aff><aff id="a3"><label>3</label><institution>Department of Stomatology, PLA Xizang Military Region General Hospital</institution>, Lhasa, Tibet,<country>People’s Republic of China</country></aff><aff id="a4"><label>4</label><institution>Department of Stomatology</institution>, PLA 301th Hospital, Beijing,<country>People’s Republic of China</country></aff></contrib-group><author-notes><corresp id="c1"><label>a</label><email>Zhuojingluo@sina.com</email></corresp><corresp id="c2"><label>b</label><email>yanjin@fmmu.edu.cn</email></corresp><fn id="n1"><label>*</label><p>These authors contributed equally to this work.</p></fn></author-notes><pub-date pub-type="epub"><day>05</day><month>01</month><year>2017</year></pub-date><pub-date pub-type="collection"><year>2017</year></pub-date><volume>7</volume><elocation-id>40088</elocation-id><history><date date-type="received"><day>22</day><month>06</month><year>2016</year></date><date date-type="accepted"><day>01</day><month>12</month><year>2016</year></date></history><permissions><copyright-statement>Copyright © 2017, The Author(s)</copyright-statement><copyright-year>2017</copyright-year><copyright-holder>The Author(s)</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link></license-p></license></permissions><abstract><p>During tooth development, the jawbone interacts with dental germ and provides the development microenvironment. Jawbone-derived mesenchymal stem cells (JBMSCs) maintain this microenvironment for root and periodontium development. However, the effect of the jawbone microenvironment on periodontium tissue regeneration is largely elusive. Our previous study showed that cell aggregates (CAs) of bone marrow mesenchymal stem cells promoted periodontium regeneration on the treated dentin scaffold. Here, we found that JBMSCs enhanced not only the osteogenic differentiation of periodontal ligament stem cells (PDLSCs) but also their adhesion to titanium (Ti) material surface. Importantly, the compound CAs of PDLSCs and JBMSCs regenerated periodontal ligament-like fibers and mineralized matrix on the Ti scaffold surface, both in nude mice ectopic and minipig orthotopic transplantations. Our data revealed that an effective regenerative microenvironment, reconstructed by JBMSCs, promoted periodontium regeneration by regulating PDLSCs function on the Ti material.</p></abstract></article-meta></front><floats-group><fig id="f1"><label>Figure 1</label><caption><title>Initial adhesion and morphology of PDLSCs on Ti in indirect co-culture system.</title><p>Morphology of PDLSCs and PDLSCs indirectly co-cultured with JBMSCs/IBMSCs after 2 hours (<bold>A</bold>) and 24 hours (<bold>B</bold>) by SEM. Adhesive number of PDLSCs in indirect co-culture system were measured by counting the Hoechst-stained cells under a fluorescence microscope after 0.5 and 2 hours (<bold>C,D</bold>). The data are shown as the mean ± SD; *P < 0.05, n = 3.</p></caption><graphic xlink:href="srep40088-f1"></graphic></fig><fig id="f2"><label>Figure 2</label><caption><title>Osteogenic differentiation of PDLSCs on Ti in indirect co-culture system.</title><p>ALP staining (<bold>A</bold>) and ALP activity (<bold>C</bold>) test were performed after 1 and 2 weeks of osteogenic induction, respectively. Alizarin Red staining (<bold>A</bold>) and quantitative analysis (<bold>B</bold>) were performed after 4 weeks of osteogenic induction. The expression levels of Runx2, ALP, Col-I and periostin investigated by qRT-PCR after PDLSCs indirectly co-cultured with JBMSCs/IBMSCs on Ti. The expression levels were normalized to β-actin with osteogenic induction for 1 (<bold>D</bold>) and 2 weeks (<bold>E</bold>). The data are shown as the mean ± SD; *P < 0.05, n = 3.</p></caption><graphic xlink:href="srep40088-f2"></graphic></fig><fig id="f3"><label>Figure 3</label><caption><title>Immunohistochemical analyses of compound CAs.</title><p>Both compound CAs positively expressed ALP, fibronectin, periostin, integrinβ1 and Runx2. ALP and Runx2 indicated the osteogenic differentiation capacity. Integrinβ1 and fibronectin were the markers of bio-functions. Periostin was a special marker of periodontal ligament.</p></caption><graphic xlink:href="srep40088-f3"></graphic></fig><fig id="f4"><label>Figure 4</label><caption><title>Microscopic appearance of the scaffold materials and the adhesion of the compound CAs to the scaffolds.</title><p>SEM images of CBB showed a porous structure, while Ti-implant showed a micro-pore facial structure (<bold>A,B</bold>). The attachment of compound CAs on the surface of CBB or Ti-implant was analyzed by SEM (<bold>C–F</bold>).</p></caption><graphic xlink:href="srep40088-f4"></graphic></fig><fig id="f5"><label>Figure 5</label><caption><title>Periodontium tissue regeneration of compound CAs in nude mice ectopic transplantation.</title><p>Periodontium regeneration of human compound CAs, and the control group was analyzed by VVG (<bold>A</bold>) and Masson trichrome (<bold>B</bold>) staining. Reconstructive images showed mineralized matrix deposition on Ti (<bold>C</bold>). The quantitative assay of reconstruction images showed the average difference of mineralized matrix on Ti was significant among three groups (P < 0.05) (<bold>D</bold>). The red arrows indicate blood vessel. The data are shown as the mean ± SD; *P < 0.05, n = 3.</p></caption><graphic xlink:href="srep40088-f5"></graphic></fig><fig id="f6"><label>Figure 6</label><caption><title>Periodontium tissue regeneration of compound CAs in minipig orthotopic transplantation.</title><p>The transplantation surgery on minipigs was shown (<bold>A</bold>). Periodontium regeneration of pig compound CAs was analyzed by VVG (<bold>B</bold>) and Masson trichrome (<bold>C</bold>) staining. Reconstructive images showed mineralized matrix position on the Ti (<bold>D</bold>). The quantitative assay of reconstruction images showed the average difference of mineralized matrix on Ti was significant among three groups (P < 0.05) (<bold>D</bold>). The red arrows indicate blood vessel. The data are shown as the mean ± SD; *P < 0.05, n = 3.</p></caption><graphic xlink:href="srep40088-f6"></graphic></fig><table-wrap position="float" id="t1"><label>Table 1</label><caption><title>Compound CAs coating Ti in nude mice ectopic transplantation and minipig orthotopic transplantation success rate.</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50">Group</th><th align="center" valign="top" charoff="50">hJBMMSCs/hPDLSCs with Ti</th><th align="center" valign="top" charoff="50">hIBMMSCs/hPDLSCs with Ti</th><th align="center" valign="top" charoff="50">pJBMMSCs/hPDLSCs with Ti</th><th align="center" valign="top" charoff="50">pIBMMSCs/hPDLSCs with Ti</th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">Implant</td><td align="center" valign="top" charoff="50">10</td><td align="center" valign="top" charoff="50">10</td><td align="center" valign="top" charoff="50">10</td><td align="center" valign="top" charoff="50">10</td></tr><tr><td align="left" valign="top" charoff="50">Die</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td></tr><tr><td align="left" valign="top" charoff="50">Lost</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">1</td><td align="center" valign="top" charoff="50">0</td><td align="center" valign="top" charoff="50">0</td></tr><tr><td align="left" valign="top" charoff="50">Harvest</td><td align="center" valign="top" charoff="50">9</td><td align="center" valign="top" charoff="50">8</td><td align="center" valign="top" charoff="50">10</td><td align="center" valign="top" charoff="50">10</td></tr><tr><td align="left" valign="top" charoff="50">Regeneration</td><td align="center" valign="top" charoff="50">8</td><td align="center" valign="top" charoff="50">7</td><td align="center" valign="top" charoff="50">8</td><td align="center" valign="top" charoff="50">6</td></tr><tr><td align="left" valign="top" charoff="50">Success rate</td><td align="center" valign="top" charoff="50">88.9%</td><td align="center" valign="top" charoff="50">87.5%</td><td align="center" valign="top" charoff="50">80.0%</td><td align="center" valign="top" charoff="50">60.0%</td></tr></tbody></table></table-wrap><table-wrap position="float" id="t2"><label>Table 2</label><caption><title>Primer Sequences.</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="left"></col><col align="left"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50">Gene</th><th align="left" valign="top" charoff="50">Forward</th><th align="left" valign="top" charoff="50">Reverse</th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">RUNX2</td><td align="left" valign="top" charoff="50">5′-CCCGTGGCCTTCAAGGT-3′</td><td align="left" valign="top" charoff="50">5′-CGTTACCCGCCATGACAGTA-3′</td></tr><tr><td align="left" valign="top" charoff="50">Periostin</td><td align="left" valign="top" charoff="50">5′-GCTGCCATCACATCGGACATA-3′</td><td align="left" valign="top" charoff="50">5′-GCTCCTCCCATAATACTCAGAACA-3′</td></tr><tr><td align="left" valign="top" charoff="50">COL-I ALP β-ACTIN</td><td align="left" valign="top" charoff="50">5′-CCAGAAGAACTGGTACATCAGCAA-3′ 5′-TAAGGACATCGCCTACCAGCTC-3′ 5′-TGGCACCCAGCACAATGAA-3′</td><td align="left" valign="top" charoff="50">5′-CGCCATACTCGAACTGGAATC-3′ 5′-TCTTCCAGGTGTCAACGAGGT-3′ 5′-CTAAGTCATAGTCCGCCTAGAGCA-3′</td></tr></tbody></table></table-wrap></floats-group></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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